ORIGINAL ARTICLE

Age and growth in three populations of Dosinia exoleta(Bivalvia: Veneridae) from the Portuguese coast

Paula Moura • Paulo Vasconcelos • Miguel B. Gaspar

Received: 31 October 2012 / Revised: 25 February 2013 / Accepted: 4 March 2013 / Published online: 20 March 2013

� Springer-Verlag Berlin Heidelberg and AWI 2013

Abstract The present study aimed at estimating the age

and growth in three populations of Dosinia exoleta from

the Portuguese coast (Aveiro in the north, Setubal in the

southwest and Faro in the south). Two techniques were

compared to ascertain the most suitable method for ageing

D. exoleta. Growth marks on the shell surface and acetate

peel replicas of sectioned shells were the techniques

applied. Two hypotheses were tested: growth parameters

present latitudinal variation along the Portuguese coast;

growth parameters are influenced by the fishing exploita-

tion. Shell surface rings proved inappropriate for ageing

this species, whereas acetate peels provided realistic esti-

mates of the von Bertalanffy growth parameters (K, L? and

t0). A latitudinal gradient in growth rate was detected, with

a clear southward increase in the growth coefficient (K) of

D. exoleta (Faro [ Setubal and Aveiro) indicating that

warmer waters in southern Portugal provide optimal con-

ditions for the growth of this species. Fishing exploitation

in northern Portugal targets larger individuals and leaves

behind a younger population of smaller individuals,

decreasing the asymptotic shell length (L?) of D. exoleta

from Aveiro. The overall growth performance was com-

pared among populations of D. exoleta and with other

venerid species worldwide.

Keywords Dosinia exoleta � Age � Growth �Latitudinal variation � Fishing effects � Portugal

Introduction

The rayed artemis or mature dosinia (Dosinia exoleta

Linnaeus, 1758) is distributed from the Norwegian and

Baltic Seas, southwards to the Iberian Peninsula, into the

Mediterranean, and along the western coast of Africa to

Senegal and Gabon (Tebble 1966). This species burrows

deeply in sand, mud and gravel bottoms, from the intertidal

zone to 70 m depth (Poppe and Goto 1993; Macedo et al.

1999), but can be found up to 150 m depth (Anon 2001). In

Portugal, D. exoleta is among the target species of the

bivalve dredging fleet operating in the northern coast,

whereas along the southwestern and southern coasts, it

constitutes a by-catch species of the dredge fishery (Gaspar

et al. 2007). Fishery exploitation in the northern coast

started around 2007 and since then annual landings ranged

between a maximum of 37.0 tons in 2007 and a minimum

of 9.4 tons in 2010 (DGPA 2012). The latest statistics

available on the landings of D. exoleta in northern Portugal

(Matosinhos wholesale market) reported total landings of

15.3 tons in 2011, corresponding to an overall value for

first sale of 15.3 thousand euro (DGPA 2012).

Knowledge on the age and growth of commercially

exploited bivalve species is a crucial requirement for the

successful management of the fishery (Gaspar et al. 2004).

In bivalves, growth rings on the shell surface have been

widely used to make inferences about age and growth rate

(Deval 2001). Although being the most quick and economic

method, in some species it is difficult to discern real seasonal

growth rings from false rings caused by gonad development

and spawning, diseases, extreme temperatures, storms and

Communicated by Franke.

P. Moura � P. Vasconcelos � M. B. Gaspar (&)

Instituto Portugues do Mar e da Atmosfera, I.P./IPMA,

Avenida 5 de Outubro s/n, 8700-305 Olhao, Portugal

e-mail: mbgaspar@ipma.pt

P. Vasconcelos

Departamento de Biologia, Centro de Estudos do Ambiente e do

Mar (CESAM), Universidade de Aveiro, Campus de Santiago,

3810-193 Aveiro, Portugal

123

Helgol Mar Res (2013) 67:639–652

DOI 10.1007/s10152-013-0350-7

damage during dredging (Gaspar et al. 1995, 2004; Rich-

ardson 2001; Keller et al. 2002; Moura et al. 2009). These

constraints have been overcome by analysing internal shell

microgrowth banding patterns revealed in acetate peel rep-

licas of sectioned shells (Jones et al. 1990; Ramon and

Richardson 1992; Richardson 2001). Although being a time-

consuming method, internal growth lines visible in acetate

peel replicas generally provide a reliable record of the age

and growth history of individuals (Anwar et al. 1990).

However, some problems in the identification of the annual

ring may also occur, especially in long-lived species. In

older specimens, the umbonal region is usually eroded,

making impossible to identify the first growth rings (Gaspar

et al. 2004). In addition, in older individuals growth

becomes slower and the later growth rings are deposited

very close together at the shell margin, making them hardly

discernible (Deval and Oray 1998; Ezgeta-Balic et al. 2011).

Furthermore, in some years clearly defined rings may not be

formed (Anwar et al. 1990). In some species, age can also be

estimated by counting the growth lines visible in acetate

peel replicas of the umbonal region of the shell (e.g. Anwar

et al. 1990; Ridgway et al. 2011; Peharda et al. 2012).

Information on the age and growth rate of D. exoleta is

very scarce and limited to studies on population dynamics

performed in Norway by Tunberg (1979). Initially, this

author attempted to find annually deposited growth marks

in the shells, using surface rings and acetate peels, but both

ageing techniques were unsuccessful (Tunberg 1979).

Later, an in situ experiment with marked individuals was

performed, but results were not satisfactory due to distur-

bance of the studied specimens and to the weakness of the

regression analysis (Tunberg 1983a). Once again, both

surface rings and acetate peels were analysed; however, it

was impossible to establish an acceptable correlation

between the number of growth marks and individual age

(Tunberg 1983a).

Taking into account the current scarcity of information,

this study aimed at improving the knowledge on the age

and growth of D. exoleta by providing data on shell

banding, age and growth rate estimates for three popula-

tions from the Portuguese coast (Aveiro in the north,

Setubal in the southwest and Faro in the south). Two

techniques (surface rings and acetate peels) were employed

and compared in order to ascertain which is the most

suitable for ageing this species. This study allowed

assessing the occurrence of latitudinal variation in the

growth parameters of D. exoleta along the Portuguese

coast, as well as comparing growth parameters between

fishery-exploited (Aveiro) and unexploited (Setubal and

Faro) populations of this species. Finally, the overall

growth performance (OGP) was compared among popu-

lations of D. exoleta and with analogous information

available for other venerid species worldwide.

Materials and methods

Samples of D. exoleta were collected between May and

June 2010 in three areas along the Portuguese coast: Aveiro

(408590–418030N) in the northern coast, Setubal (388230–388270N) in the southwestern coast and Faro (368580–368590N) in the southern coast (Fig. 1). Individuals were

caught by the IPMA’s RV ‘‘Diplodus’’ operating bivalve

dredges on sandy bottoms between 8 and 12 m depth in the

southern coast, 8 and 15 m depth in the southwestern coast

and between 15 and 30 m depth in the northern. Following

the usual fishing procedures, the dredges were towed for

15 min at a constant speed of 2 knots. The dredges used

were identical to those operated by the commercial fleet. In

brief, the dredge weighs around 40 kg and consists of a

rigid iron structure with a toothed lower bar (15 cm tooth

length with an angle of 208). The catch is retained in a net

bag 2.5 m long with diamond mesh size of 25 mm for

further details on the dredge design, characteristics and

dimensions, see (Gaspar et al. 2003); (Leitao et al. 2009).

In order to assess its influence on the growth of

D. exoleta, data on seawater temperature along the Portuguese

coast were provided by the Hydrographical Institute (IH).

For this purpose were gathered data monitored during 2010

by the oceanographic buoys closest to the bivalve collect-

ing sites (buoys of Leixoes in the northern coast, Sines in

the southwestern coast and Faro in the southern coast).

Mean annual temperature was compared between study

areas through analysis of variance (ANOVA). If ANOVA

assumptions (normality of data and homogeneity of vari-

ances) were not met, the nonparametric Kruskal–Wallis

test (ANOVA on ranks) was performed. Whenever sig-

nificant differences were detected by ANOVA or Kruskal–

Wallis test, pairwise multiple comparisons were made

using Tukey or Dunn’s tests, respectively (Zar 1999).

Statistical analyses were performed with the software

package SigmaStat� (version 3.5) with significance con-

sidered for P \ 0.05.

In the laboratory, a total of 50 individuals from each

collecting site were measured for shell length (SL) (max-

imum distance along the anterior–posterior axis) to

the nearest 0.1 mm using a digital calliper. Specimens

analysed were within the following SL (ranges Ave-

iro = 40.4–46.8 mm (42.5 ± 1.7 mm); Setubal = 41.7–

52.0 mm (46.7 ± 3.1 mm); Faro = 36.9–44.3 mm

(41.0 ± 2.1 mm)). Subsequently, for estimating age and

growth, the rings deposited on the external surface of the

shells were counted and measured with the digital calliper.

In addition, the internal structure of each shell was ana-

lysed using acetate peel replicas of polished and etched

sections of resin-embedded valves, following the technique

previously adopted with success in other commercially

exploited bivalve species from the Portuguese coast (for

640 Helgol Mar Res (2013) 67:639–652

123

further details see Gaspar et al. 1995, 2002, 2004; Moura

et al. 2009). Based on previous studies with sympatric

bivalve species from the Portuguese coast, such as Callista

chione (Moura et al. 2009) and Chamelea gallina (Gaspar

et al. 2004), it was assumed that the growth marks in the

shells of D. exoleta are annual, being deposited in late

autumn–early winter when shell growth is slower. Each

growth ring observed in the acetate peel was marked on the

glass slide. After digitising the entire acetate peel and

respective marks, the distance between the umbo and each

growth ring was measured to the nearest 0.1 mm using the

digital image analysis software ImageJ (version 1.43). In

both techniques (shell surface and acetate peels), counting

and measuring of growth rings were made by two inde-

pendent observers and a second reading was performed

whenever numbers did not coincide. Since the measure-

ments in acetate peels are relative to shell height (SH), data

were converted into SL using the following morphometric

relationship (n = 259, r = 0.990; Gaspar et al. 2002):

Log SH ¼ �0:040þ 1:012 Log SL

Von Bertalanffy growth functions (VBGF) were fitted

separately to the age–length data obtained using the two

ageing methods (shell surface rings and internal growth

marks). An iterative curve fitting procedure employ-

ing nonlinear least-squares regression (Gauss–Newton

method) provides estimates of the growth coefficient

(K), asymptotic SL (L?) and theoretical age at SL (zero

(t0), through the following equation (von Bertalanffy

1938):

Lt ¼ L1½1� e�Kðt�t0Þ�

Linear methods commonly used in the statistical

comparison of growth data (ANCOVA or ANOVA)

Setúbal

10

15

20

25

30

J F M A M J J A S O N D

Seaw

ater

tem

pera

ture

(ºC

)

10

15

20

25

30

Seaw

ater

tem

pera

ture

(ºC

)

10

15

20

25

30

Seaw

ater

tem

pera

ture

(ºC

)Faro:

Setúbal:

Aveiro:

20.2 3.1ºC (14.6 – 26.6ºC)

17.3 1.2ºC (15.1 – 21.2ºC)

15.4 1.8ºC (11.4 – 20.4ºC)

9

42

38

8

40

Lat

itud

e (º

N)

Longitude (ºW)

±

±

±

Aveiro

Faro

Port

ugal

N

Fig. 1 Geographical location and seawater temperature at the

collecting sites for Dosinia exoleta along the Portuguese coast

(Aveiro, Setubal and Faro). Shadow squares denote the collecting

sites. Seawater temperature monitored during 2010 by the

oceanographic buoys closest to the collecting sites. Error bars

represent monthly standard deviation, and interrupted lines represent

annual mean and range (minimum–maximum) in seawater

temperature

Helgol Mar Res (2013) 67:639–652 641

123

cannot be employed on the VBGF because of its nonlinear

formulation and high degree of correlation between its

three parameters (K, L? and t0) (Chen et al. 1992).

Comparisons of VBGF can be performed using two general

approaches, either by testing individual parameters or

by using likelihood ratio statistics. In the present case,

D. exoleta growth equations were compared between

populations (Aveiro, Setubal and Faro) using likelihood

ratio tests (Kimura 1980; Cerrato 1990). This method allows

testing several hypotheses to compare two growth equations,

by analysing each growth parameter separately or all growth

parameters simultaneously. Fitting and comparison of VBGF

were performed using the packages ‘‘nlstools’’ (Baty and

Delignette-Muller 2011), ‘‘car’’ (Fox and Weisberg 2011) and

‘‘fishmethods’’ (Nelson 2011) of the free software R (version

2.14.1) (R Development Core Team 2011).

Individual growth is a nonlinear process that must be

described by multiparameter nonlinear models (such as the

VBGF), making it difficult to compare growth among

different taxa in a definite and statistically proper way

(Brey 1999). To overcome this difficulty, several growth

performance indices have been developed. In the present

study,OGP (P) (Pauly 1979) was employed to compare the

growth parameters estimated for D. exoleta in the present

study with those available in the literature for other venerid

species, using the following equation:

P ¼ LogðK � L31Þ

Results

Mean annual seawater temperature (Fig. 1) was signifi-

cantly different (H = 4292.159, P \ 0.001) between col-

lecting sites: Aveiro = 15.4 ± 1.8 �C (11.4–20.4 �C),

Setubal = 17.3 ± 1.2 �C (15.1–21.2 �C) and Faro =

20.2 ± 3.1 �C (14.6–26.6 �C). There was a remarkable

thermal range between the northernmost site (minimum of

11.4 �C in December 2010 in Aveiro) and the southernmost

site (maximum of 26.6 �C in August 2010 in Faro). As

expected, seawater temperature displayed a clear northward

decreasing trend: Aveiro \ Setubal (Q = 30.519, P \ 0.05)

and Setubal \ Faro (Q = 31.826, P \ 0.05).

Shell surface rings and acetate peel replicas of

D. exoleta shell sections are presented in Fig. 2. Observation

of the outer prismatic layer revealed distinct growth pat-

terns deposited parallel to the ventral edge of the shell, but

defined lines were not found in the umbonal region. The

growth marks formed a growth ring in the outer shell

surface that was associated with a cleft, and occasionally,

two clefts were associated with an annual growth ring

(Fig. 2a). In the acetate peels, the gradual decrease in the

growth increment zone was the key to distinguish annual

growth rings from false rings (caused by stress or shell

damage). The former were characterised by the progressive

narrowing of growth bands (Fig. 2b), whereas the latter

were characterised by the sudden interruption of the natural

growth pattern. In false rings, it is also possible to observe

a cleft in the shell surface, but the acetate peel does not

display narrowing in the microgrowth increments (Fig. 2c).

The mean length-at-age and respective VBGF of

D. exoleta populations from Aveiro, Setubal and Faro,

estimated using both ageing techniques (surface rings and

acetate peels), are compiled in Table 1. The VBG param-

eters obtained from surface rings (Fig. 2d) displayed

unrealistically high asymptotic SL’s (Aveiro: L? =

76.6 mm; Setubal: L? = 65.8 mm; Faro: L? = 53.3 mm),

and therefore, this ageing method was considered inap-

propriate for estimating D. exoleta age and growth. The

comparison between shell surface rings and microgrowth

patterns revealed by the acetate peel replica of the same

individual (Fig. 2a, d) supports this conclusion. In contrast,

the VBG parameters (K, L? and t0) estimated using the

acetate peels were fairly realistic (Table 1). Accordingly,

VBGF based on growth marks revealed in the acetate

peels of the three populations of D. exoleta from the Por-

tuguese coast (Aveiro, Setubal and Faro) are presented in

Fig. 3.

The likelihood ratio tests for comparison of VBG

parameters between populations of D. exoleta are compiled

in Table 2. When all VBG parameters (K, L? and t0) were

analysed simultaneously (H4:VBGF), all growth curves

displayed highly significant differences (P \ 0.001)

between the populations from Aveiro, Setubal and Faro.

When each VBG parameter was analysed separately, it was

possible to determine which parameter (K, L? or t0) was

significantly different among populations. The growth

coefficient (H1: K) was significantly higher in D. exoleta

from Faro (K = 0.50 year-1) than in the populations from

Aveiro (K = 0.28 year-1) and Setubal (K = 0.30 year-1).

The asymptotic SL (H2:L?) was slightly higher in

D. exoleta from Setubal (L? = 47.1 mm), although not sta-

tistically different from those in the populations from Faro

(L? = 42.9 mm) and Aveiro (L? = 43.9 mm). Finally,

the theoretical age at SL (zero (H3:t0), considered the VBG

parameter with lower biological significance, only dis-

played significant differences between the populations from

Faro (t0 = -0.07 years) and Aveiro (t0 = 0.27 years)

(Table 2). Overall, growth rates of D. exoleta presented a

latitudinal gradient along the Portuguese coast and were

directly related to mean annual seawater temperature at the

collecting sites. Indeed, the growth rate was highest in the

southernmost and warmest site (Faro: K = 0.50 year-1,

temperature = 20.2 �C) and lowest in the northernmost and

coldest site (Aveiro: K = 0.28 year-1, temperature =

15.4 �C), with the transitional population at an intermediate

position (Setubal: K = 0.30 year-1, temperature = 17.3 �C).

642 Helgol Mar Res (2013) 67:639–652

123

Two VBG parameters (K and L?) were applied to cal-

culate the OGP of D. exoleta along the Portuguese coast.

The OGP values obtained for the three studied populations

were P = 4.374 in Aveiro, P = 4.496 in Setubal and

P = 4.597 in Faro. The VBG parameters and correspond-

ing OGP values for D. exoleta and other venerid bivalve

species are compiled in Table 3 and compared among

different taxa in the auximetric grid presented in Fig. 4.

Fig. 2 Acetate peel replicas and surface growth rings in the shell of

Dosinia exoleta: a Acetate peel of sectioned valve illustrating the

sequential deposition of growth marks during ontogeny (from right to

left). Annual growth rings are associated with one (single arrow) or

two (double arrows) clefts on the shell surface. b Annual growth

mark with the formation of one cleft (arrow), being possible to

observe a slow-growth band where microgrowth increments become

narrow. c False growth ring (arrow) without narrowing of micro-

growth increments. d Comparison between growth rings observed on

the shell surface and growth marks revealed by the acetate peel

replica of the same shell (a). PL outer prismatic layer, MN middle

nacreous layer, IN inner nacreous layer, P periostracum, U umbo

Helgol Mar Res (2013) 67:639–652 643

123

Discussion

Age and growth of D. exoleta were more accurately esti-

mated based on internal growth marks revealed in acetate

peel replicas of sectioned shells than directly from surface

growth rings. Although quick and economic, the exami-

nation of surface rings proved to be inadequate and unre-

liable for ageing D. exoleta. The unrealistic VBG

parameters obtained from surface rings were already

expected, because the growth rate is slower in older indi-

viduals making it difficult to distinguish and measure sur-

face rings closer to the edge of the shell (Deval 2001;

Gaspar et al. 2004; Moura et al. 2009). Differences

Table 1 Mean shell length-at-age (SL) and von Bertalanffy growth function (VBGF) of D. exoleta from three locations along the Portuguese

coast (Aveiro, Setubal and Faro) obtained using two ageing techniques (shell surface rings and acetate peels)

Location Age (years) Surface rings Acetate peels

Number of observations Mean SL (mm) Number of observations Mean SL (mm)

Aveiro (N) 1 50 11.2 ± 1.5 (7.5–13.5) 50 12.7 ± 1.6 (10.7–15.4)

2 50 16.4 ± 1.0 (14.3–18.0) 50 21.8 ± 1.3 (19.5–23.6)

3 50 20.7 ± 1.4 (18.1–23.4) 50 26.1 ± 0.9 (24.8–28.1)

4 50 24.8 ± 1.0 (22.8–26.5) 50 30.7 ± 1.2 (28.7–32.7)

5 50 28.3 ± 1.2 (27.0–30.7) 50 33.5 ± 1.3 (31.5–36.6)

6 50 33.3 ± 1.0 (31.2–34.9) 50 36.2 ± 0.7 (34.7–37.1)

7 50 36.6 ± 0.8 (35.2–38.0) 43 38.5 ± 0.9 (36.8–40.2)

8 48 39.4 ± 0.8 (37.7–40.8) 18 40.1 ± 1.2 (38.1–41.7)

9 21 41.3 ± 1.0 (40.0–43.0)

10 5 43.7 ± 1.3 (42.8–44.6)

VBGF Lt = 76.6 [(1-e-0.08(t?0.97)] Lt = 43.9 [(1-e-0.28(t?0.27)]

Setubal (SW) 1 50 9.5 ± 1.0 (8.1–11.4) 50 13.2 ± 1.1 (11.5–15.6)

2 50 14.4 ± 1.4 (12.1-17.1) 50 19.8 ± 2.8 (14.3–23.5)

3 50 19.5 ± 1.4 (17.4–22.1) 50 27.6 ± 2.7 (23.0–34.1)

4 50 23.9 ± 1.8 (20.2–26.0) 50 33.6 ± 3.1 (28.3–40.9)

5 50 29.1 ± 1.5 (27.2–31.6) 50 37.1 ± 3.6 (31.1–45.4)

6 50 33.3 ± 1.4 (31.0–35.1) 46 39.2 ± 2.8 (34.1–44.3)

7 50 36.4 ± 1.3 (34.2–37.9) 29 40.1 ± 2.7 (36.0–43.0)

8 47 38.9 ± 1.4 (36.4–41.2) 25 42.3 ± 3.1 (37.5–45.8)

9 43 41.4 ± 1.2 (38.1–43.0) 11 44.4 ± 4.9 (38.8–47.4)

10 30 43.9 ± 0.5 (43.1–44.5)

11 13 46.1 ± 1.2 (44.6–47.3)

VBGF Lt = 65.8 [(1-e-0.11(t?0.37)] Lt = 47.1 [(1-e-0.30(t?0.2)]

Faro (S) 1 50 13.8 ± 1.8 (10.5–17.7) 50 16.0 ± 2.4 (12.2–19.3)

2 50 20.4 ± 2.9 (15.6–28.0) 50 26.6 ± 2.6 (22.4–29.9)

3 50 27.9 ± 3.5 (23.6–34.9) 50 33.1 ± 1.7 (30.0–35.8)

4 50 34.4 ± 2.9 (29.8–38.9) 45 36.9 ± 1.4 (35.0–39.0)

5 40 37.9 ± 2.6 (33.7–42.0) 17 39.2 ± 0.9 (38.1–40.9)

6 27 39.5 ± 3.0 (35.1–43.2) 1 41.2 ± 0.0 (41.2–41.2)

VBGF Lt = 53.3 [(1-e-0.23(t?0.23)] Lt = 42.9 [(1-e-0.50(t-0.07)]

Data presented as mean ± SD and size range

0

10

20

30

40

50

0 1 2 3 4 5 6 7 8 9 10

Age (years)

Shel

l len

gth

(mm

)

Aveiro:

Setúbal:

Faro:

Lt = 43.88 [(1 - e –0.28 (t+0.27)]; r = 0.989

Lt = 47.08 [(1 - e –0.30 (t+0.02)]; r = 0.955

Lt = 42.93 [(1 - e –0.50 (t-0.07)]; r = 0.976

Fig. 3 Von Bertalanffy growth functions (VBGF) for the three

populations of D. exoleta from the Portuguese coast (Aveiro, Setubal

and Faro), based on growth marks revealed in the acetate peels

644 Helgol Mar Res (2013) 67:639–652

123

between surface and internal growth rings were also

observed in Macoma balthica. In this case, the number of

annual lines obtained from external rings was always

higher compared to the internal rings determined from the

acetate peel replicas (Cardoso et al. 2012).

Examination of acetate peel replicas of D. exoleta

allowed identifying different phases of shell growth,

namely narrow dark lines (slow growth) separated by wider

microgrowth increments (rapid growth). Other bivalve

species from the Portuguese coast showed the same growth

pattern, which has been associated with annual shell

growth, including Donax trunculus (Gaspar et al. 1999),

C. gallina (Gaspar et al. 2004) and C. chione (Moura et al.

2009). Periods of shell slow growth might be caused by

low metabolic rates related to low seawater temperature

(Lomovasky et al. 2002), lack of food (Arneri et al. 1998)

and/or by diversion of metabolic products into gamete

production (Lomovasky et al. 2002). Narrow bands corre-

sponding to shell slow growth are often followed by a

reduction in the peripheral layer of the shell, thus forming

a cleft (Leontarakis and Richardson 2005). Indeed, in

D. exoleta the narrowing of microgrowth bands also appeared

to always match with a cleft on the shell surface. Moreover,

occasionally two narrow bands were deposited very close

together (appearing like a double band) and were reflected

by the occurrence of two clefts on the shell surface. This

phenomenon has also been detected in C. gallina by

Ramon and Richardson (1992) and Gaspar et al. (2004).

The occurrence of double clefts on the shell surface further

strengthens the acetate peel technique as the most adequate

and accurate method for ageing D. exoleta. The examina-

tion of acetate peel replicas of sectioned shells also allowed

detecting several clefts associated with a sudden interrup-

tion of the natural growth pattern and that were interpreted

as false rings. On the shell surface, false rings induced by

gonad development and spawning, diseases, extreme tem-

peratures, storms, predation or dredging are in most cases

indistinguishable from seasonal growth rings (Gaspar et al.

2004). In some bivalve species, age can be estimated by

counting the number of growth rings deposited in the

umbonal region of the shell (e.g. Anwar et al. 1990;

Ridgway et al. 2011; Cardoso et al. 2012; Peharda et al.

2012). However, this was unfeasible with D. exoleta, since

in most acetate peels the growth rings in the umbonal

region were absent or very difficult to discern. Similarly, in

C. gallina, the growth bands in the umbonal region were

only observed in a limited number of individuals, making

this method inappropriate for ageing this species (Dalgic

et al. 2010).

The VBGF of the population of D. exoleta from Setubal

displayed the highest shell asymptotic length (L?), fol-

lowed by the population from Aveiro. The population from

Faro presented the lowest L?, but in contrast, showed the

highest growth rate (K). The populations from Setubal and

Aveiro showed lower and similar growth rates (K). These

different growth features between populations of D. exoleta

are probably a consequence of the fishing exploitation and

certainly also reflect different environmental conditions

between the collecting sites, namely in terms of seawater

temperature.

Along the Portuguese coast, only the population of

D. exoleta from Aveiro is exploited, whereas in Setubal

and Faro, it constitutes a by-catch species of the dredge

fishery (sorted on-board and discarded alive in the fishing

beds). Therefore, the fishery targeting D. exoleta in Aveiro

certainly causes a decline in the proportion of larger indi-

viduals (decreasing L?). Studies on the fishing impact on

bivalve growth were relatively scarce but have increased

recently. For instance, fishery exploitation appears to have

decreased L? and Lmax of Anadara tuberculosa from Bahıa

Magdalena, Mexico (Felix-Pico et al. 2009). Similarly, the

decline in the abundance and sizes of A. tuberculosa over

the years in Costa Rica suggest that the fishing pressure on

this species is too high (Campos et al. 1990; Silva-Bena-

vides and Bonilla-Carrion 2001).

The rayed artemis (or mature dosinia) is distributed

along a widespread latitudinal range, from northern Euro-

pean coasts (probable northern limit in Finnmark)

Table 2 Likelihood ratio tests for comparing the von Bertalanffy growth parameters of three populations of Dosinia exoleta from the Portuguese

coast (Aveiro, Setubal and Faro)

Locations H1:K H2:L? H3:t0 H4:VBGF

Aveiro versus. Setubal v2 = 0.12

P = 0.729 ns

v2 = 2.11

P = 0.146ns

v2 = 1.99

P = 0.158ns

v2 = 39.77

P \ 0.001

Aveiro versus. Faro v2 = 18.97

P \ 0.001

v2 = 0.37

P = 0.543ns

v2 = 7.05

P = 0.008**

v2 = 198.91

P \ 0.001

Setubal versus. Faro v2 = 6.52

P = 0.011*

v2 = 2.47

P = 0.116ns

v2 = 0.23

P = 0.632ns

v2 = 68.90

P \ 0.001

ns not significant

* P \ 0.05; ** P \ 0.01

Helgol Mar Res (2013) 67:639–652 645

123

Table 3 Comparison of the von Bertalanffy growth parameters and corresponding overall growth performance between Dosinia exoleta and

other venerid species worldwide

Species K (year-1) L? (mm) P Ageing

method

Study area Reference

D. exoleta (9, 1) 0.28 43.88 4.374 AP Aveiro, Portugal (Atlantic Ocean) Present study

D.exoleta (9, 2) 0.30 47.08 4.496 AP Setubal, Portugal (Atlantic Ocean) Present study

D. exoleta (9, 3) 0.50 42.93 4.597 AP Faro, Portugal (Atlantic Ocean) Present study

D. exoleta (9, 4) 0.36 51.3 4.687 MR Eggholmane, Norway (Atlantic Ocean) Tunberg (1983a)

D. lupinus (9, 5) 0.36 36.0 4.225 SR Eggholmane, Norway (Atlantic Ocean) Tunberg (1983b)

D. nipponica (9 ,6) 0.159 78.95 4.893 AP Wakkanai Port, Japan (Pacific Ocean) Tanabe and Oba (1988)

D. nipponica (9, 7) 0.203 74.46 4.923 AP Hakodate Bay, Japan (Pacific Ocean) Tanabe and Oba (1988)

D. nipponica (9, 8) 0.262 61.06 4.776 AP Tokyo Bay, Japan (Pacific Ocean) Tanabe and Oba (1988)

D. nipponica (9, 9) 0.295 55.46 4.702 AP Seto Inland Sea, Japan (Pacific Ocean) Tanabe and Oba (1988)

D. nipponica (9, 10) 0.403 76.44 5.255 AP Ariake Bay, Japan (Pacific Ocean) Tanabe and Oba (1988)

A. antiqua (d, 11) 0.183 80.00 4.972 MR Chiloe, Chile (Pacific Ocean) Clasing et al. (1994)

A. umbonella (s, 12) 0.28 58.0 4.737 LF Park-e-Dolat, Iran (Persian Gulf) Saeedi et al. (2010)

A. umbonella (s, 13) 0.29 62.0 4.840 LF Park-e-Qadir, Iran (Persian Gulf) Saeedi et al. (2010)

C. brevisiphonata

(j, 14)

0.202 101.8 5.329 SR, CS Ussuri Bay, Russia (Sea of Japan) Selin and Selina (1988)

C. brevisiphonata

(j, 15)

0.177 102.2 5.276 SR, CS Putyatin Islands, Russia (Sea of Japan) Selin and Selina (1988)

C. brevisiphonata

(j, 16)

0.147 113.4 5.331 SR, CS Vostok Bay, Russia (Sea of Japan) Selin and Selina (1988)

C. chione (j, 17) 0.24 93.0 5.286 SR, TS Gulf of Euboikos, Greece (Aegean Sea) Metaxatos (2004)

C. chione (j, 18) 0.24 62.7 4.772 AP Thassos Island, Greece (Thracian Sea) Leontarakis and Richardson

(2005)

C. chione (j, 19) 0.26 57.8 4.701 AP Thassos Island, Greece (Thracian Sea) Leontarakis and Richardson

(2005)

C. chione (j, 20) 0.15 98.1 5.151 AP Arrabida, Portugal (Atlantic Sea) Moura et al. (2009)

C. chione (j, 21) 0.18 91.1 5.134 SR Arrabida, Portugal (Atlantic Sea) Moura et al. (2009)

C. chione (j, 22) 0.25 72.4 4.977 AP Rab Island, Croatia (Adriatic Sea) Ezgeta-Balic et al. (2011)

C. chione (j, 23) 0.15 74.5 4.793 AP Pag Bay, Croatia (Adriatic Sea) Ezgeta-Balic et al. (2011)

C. chione (j, 24) 0.11 82.8 4.795 AP Kastela Bay, Croatia (Adriatic Sea) Ezgeta-Balic et al. (2011)

C. chione (j, 25) 0.34 79.3 5.229 AP Cetina Estuary, Croatia (Adriatic Sea) Ezgeta-Balic et al. (2011)

C. gallina (h, 26) 0.35 36.12 4.217 AP Valencia, Spain (Mediterranean Sea) Ramon and Richardson

(1992)

C. gallina (h, 27) 0.40 40.05 4.410 LF Valencia, Spain (Mediterranean Sea) Ramon (1993)

C. gallina (h, 28) 0.21 52.20 4.475 TS Ancona, Italy (Adriatic Sea) Polenta (1993)

C. gallina (h, 29) 0.48 41.60 4.539 TS Ancona, Italy (Adriatic Sea) Arneri et al. (1995)

C. gallina (h, 30) 0.52 39.50 4.506 TS Neretva Estuary, Croatia (Adriatic Sea) Arneri et al. (1997)

C. gallina (h, 31) 0.429 34.17 4.233 SR Turkey (Northern Marmara Sea) Deval and Oray (1998)

C. gallina (h, 32) 0.37 33.46 4.142 TS Turkey (Northern Marmara Sea) Deval (2001)

C. gallina (h, 33) 0.609 27.25 4.091 TS Russia (Northern Black Sea) Boltachova and Mazlumyan

(2001)

C. gallina (h, 34) 0.47 38.95 4.444 AP Faro, Portugal (Atlantic Ocean) Gaspar et al. (2004)

C. gallina (h, 35) 0.32 42.15 4.380 LF Faro, Portugal (Atlantic Ocean) Gaspar et al. (2004)

C. gallina (h, 36) 0.71 37.55 4.575 SR Faro, Portugal (Atlantic Ocean) Gaspar et al. (2004)

C. gallina (h, 37) 0.16 26.00 3.449 TS Yakakent, Turkey (Black Sea) Dalgic et al. (2010)

C. gallina (h, 38) 0.21 28.88 3.704 TS Inceburun, Turkey (Black Sea) Dalgic et al. (2010)

C. gallina (h, 39) 0.22 26.60 3.617 TS Cide, Turkey (Black Sea) Dalgic et al. (2010)

C. striatula (h, 40) 0.23 32.90 3.913 SR Millport, Scotland (Atlantic Ocean) Ursin (1963)

C. striatula (h, 41) 0.25 38.75 4.163 SR Bristol Channel, UK (Atlantic Ocean) Warwick et al. (1978)

646 Helgol Mar Res (2013) 67:639–652

123

(Tunberg 1984) to western African coasts, not being found

further south than Congo (Fischer-Piette 1968). This

implies that Portugal is fairly within the middle of the

latitudinal distribution of this species in the Atlantic Ocean.

It is well known that physiological processes are influenced

by the environmental conditions, namely temperature and

food availability (e.g. Clarke 1987; Sprung 1991; Masila-

moni et al. 2002), parameters that usually show an inverse

trend with latitude (Barry and Carleton 2001; Jansen et al.

2007). With increasing latitude, it has been observed an

increasing trend in reproductive effort, egg and larval size,

whereas an opposite trend has been shown for age at first

maturity, fecundity, reproductive output, growth rate and

mortality (e.g. Clarke 1987; Contreras and Jaramillo 2003;

Thatje et al. 2004; Ward and Hirst 2007; Petracco et al.

2010).

In the present study, it was also detected a latitudinal

gradient in the growth of the three populations of

D. exoleta, with growth rates (K) showing a southward

increase (Faro [ Setubal & Aveiro). Latitudinal trends in

the physiological performance of marine invertebrates are

commonly observed (Santos et al. 2011). Latitude has no

environmental meaning by itself, being a proxy of annual

solar energy input that translates mainly into average

annual seawater temperature (Heilmayer et al. 2003), but

also into primary production and related parameters. On a

geographical scale, differences in growth rate of bivalves

have been frequently associated with latitudinal gradients

in seawater temperature. Examples of this phenomenon

include C. chione (Hall et al. 1974), M. balthica (Beukema

and Meehan 1985), Mercenaria campechiensis and Merc-

enaria mercenaria (Heck et al. 2002), Mya arenaria (Ap-

peldoorn 1995), Placopecten magellanicus (MacDonald

and Thompson 1988), Tivela stultorum (Hall et al. 1974)

and Zygochlamys patagonica (Gutierrez and Defeo 2003).

In the present study along the Portuguese coast, higher

seawater temperatures were registered in the south, which

may explain the higher growth rate displayed by the pop-

ulation of D. exoleta from Faro compared to the popula-

tions from the other two collecting sites. However, the

abundance of this species in Faro is very low compared to

Setubal and Aveiro (Fig. 5) (Gaspar et al. 2010a, b, c). This

north–south decreasing trend also supports that colder

waters constitute a more suitable environment for this

species. Indeed, although showing wide thermal range, the

optimal environmental conditions for this eurythermal

species appear to be shifted northwards. Tunberg (1983a)

estimated a shell asymptotic length (L?) of 51.3 mm for

D. exoleta from Eggholmen (western Norway), but this

value was considered somewhat small compared to the

maximum SL (reached in that area, where this species is

abundant with a density of 9.9 ± 2.9 ind m-2 (Tunberg

1983a). Moreover, higher abundances were observed in

Raunefjorden (western Norway), where D. exoleta reached

an overall density of 17.1 ind m-2 (Tunberg 1984). The

higher shell asymptotic length in northern (Norway:

Table 3 continued

Species K (year-1) L? (mm) P Ageing

method

Study area Reference

E. exalbida (r, 42) 0.180 73.98 4.863 AP, IR Beagle Channel, Argentina (Atlantic

Ocean)

Lomovasky et al. (2002)

M. mercenaria (e, 43) 0.182 94.31 5.184 SR Southampton, UK (Atlantic Ocean) Hibbert (1977)

M. mercenaria (e, 44) 0.312 71.04 5.049 AP Georgia, USA (Atlantic Ocean) Walker and Tenore (1984)

M. mercenaria (e, 45) 0.260 89.40 5.269 AP Georgia, USA (Atlantic Ocean) Walker and Tenore (1984)

M. mercenaria (e, 46) 0.340 65.90 4.988 AP Georgia, USA (Atlantic Ocean) Walker and Tenore (1984)

M. mercenaria (e, 47) 0.21 73.32 4.918 CS Narragansett Bay, USA (Atlantic Ocean) Jones et al. (1989)

Tawera gayi (?, 48) 0.288 28.03 3.802 AP, MR Beagle Channel, Argentina (Atlantic

Ocean)

Lomovasky et al. (2005)

V. corrugata (m, 49) 0.31 49.98 4.588 SR Mira Estuary, Portugal (Atlantic Ocean) Guerreiro and Rafael (1995)

V. corrugata (m, 50) 0.43 45.5 4.608 SR Ria de Aveiro, Portugal (Atlantic Ocean) Maia et al. (2006)

V. corrugata (m, 51) 0.29 54.3 4.667 AP Ria de Aveiro, Portugal (Atlantic Ocean) Maia et al. (2006)

V. verrucosa (D, 52) 0.253 44.9 4.360 CS Bari, Italy (Adriatic Sea) Arneri et al. (1998)

V. verrucosa (D, 53) 0.352 54.1 4.746 CS Gulf of Manfredonia, Italy (Adriatic Sea) Arneri et al. (1998)

V. verrucosa (D, 54) 0.298 54.2 4.676 CS Gulf of Maliakos, Greece (Aegean Sea) Arneri et al. (1998)

V. verrucosa (D, 55) 0.324 52.1 4.661 CS Bay of Thessaloniki, Greece (Aegean Sea) Arneri et al. (1998)

V. verrucosa (D, 56) 0.360 43.4 4.469 CS Alexandroupolis, Greece (Aegean Sea) Arneri et al. (1998)

K growth coefficient, L? asymptotic shell length, P overall growth performance, AP acetate peels, MR mark-recapture, SR surface rings, LF length-

frequency, CS cross-sections, TS thin sections, IR isotope ratios

Helgol Mar Res (2013) 67:639–652 647

123

L? = 51.3 mm) than in southern populations (Portugal:

L? = 42.9–47.1 mm), further confirms that although this

species grows faster in warmer waters, higher latitudes

provide the most favourable environmental conditions for

the development of population of D. exoleta.

Although with a few exceptions, the general consensus

is that bivalves from low latitudes grow faster, attain a

smaller maximum size and have a shorter lifespan than

conspecifics from high latitudes (Newell 1964). In the

present study, the calculation of the OGP allowed com-

paring growth among populations of D. exoleta and with

other venerid bivalves. The values of OGP obtained for

D. exoleta along the Portuguese coast corroborate the

above-mentioned latitudinal gradient in growth and the

influence of mean annual seawater temperature at the

collecting sites Faro [ Setubal [ Aveiro. In terms of intra-

specific comparison, the only data available in the literature

on the growth of D. exoleta lead to slightly higher OGP in

Norway (P = 4.687) compared to the populations along

the Portuguese coast (P = 4.374 in Aveiro to P = 4.597 in

Faro). In general, worldwide comparisons highlight that

OGP increases with decreasing latitude, in a general trend

that is correlated with average annual seawater temperature

(Heilmayer et al. 2003). However, this trend was not

observed in the case of D. exoleta since a higher OGP was

determined for Norway compared to that obtained for the

Portuguese populations. This may be a consequence of the

method used by Tunberg (1983a) to estimate growth. This

author applied the mark-recapture method which may lead

to bias in growth estimates whenever the data set is not

representative of the full size range of the population

(Haddon 2001). The growth parameters estimated by

Tunberg (1983a) were mainly based on large individuals,

therefore are probably biased, which may have resulted in a

higher OGP for the Norwegian population of D. exoleta.

Within the genus, D. exoleta both from Portugal and

Norway has a slightly higher OGP than the sympatric

Dosinia lupinus from western Norway (P = 4.225)

(Tunberg 1983b), but lower than D. nipponica (4.702 \P \ 5.255) from the Pacific Ocean (Tanabe and Oba 1988).

In terms of inter-specific comparison, the auximetric grid

revealed that D. exoleta has an average growth perfor-

mance (within the family Veneridae). Indeed, D. exoleta is

within the range of OGP values obtained for Amiantis

umbonella, Ameghinomya antiqua, Eurhomalea exalbida,

Venerupis corrugata and Venus verrucosa (mainly between

4.5 \ P \ 5.0). In most cases, the sympatric C. gallina and

Chamelea striatula exhibited lower OGP (mostly P \ 4.5),

whereas Callista brevisiphonata and C. chione (usually

P [ 5.0) and M. mercenaria (mostly P [ 5.0) displayed

the highest growth performances within the family Ven-

eridae (Fig. 4).

The present study was the first to successfully estimate

age and growth of D. exoleta by using the acetate peel

technique, thus making available realistic growth parame-

ters (K and L?) for this species. Furthermore, the present

study showed some differences between the growth

parameters of the three populations. Results suggest that

growth is influenced by geographical distribution and

probably also by fishing exploitation. In general, the lati-

tudinal gradient in the growth features of the three popu-

lations revealed that, besides growing faster in warm

-1.0

-0.8

-0.6

-0.4

-0.2

0.0

4.0 4.5 5.0 5.5 6.0 6.5

Log L ∞3

Log

K

P = 5.0 P = 5.5P = 4.5P = 4.0

Fig. 4 Auximetric grid for comparison of OGP between D. exoleta

and other venerid species worldwide. Diagonal lines denote OGP

isolines, symbols and numbers refer to the species listed in Table 3

(multiplication symbol, Dosinia spp.; filled circle symbol, Ameghi-

nomya sp.; open circle symbol, Amiantis sp.; filled square symbol,

Callista spp.; open square symbol, Chamelea spp.; filled diamond

symbol, Eurhomalea sp.; open diamond symbol, Mercenaria sp.; plus

symbol, Tawera sp., filled triangle symbol, Venerupis sp.; open

triangle symbol, Venus sp.). Shadow circles denote D. exoleta

populations from the Portuguese coast (Aveiro, Setubal and Faro)

648 Helgol Mar Res (2013) 67:639–652

123

waters, colder environments are beneficial for this species.

It also seems that fishing exploitation affects the asymp-

totic SL of the populations of D. exoleta (decreasing L?),

but further investigation should be performed to confirm

this hypothesis. Knowledge on the age and growth of

exploited bivalve species is fundamental for the proposal of

Fig. 5 Spatial distribution, abundance (g 5 min tow-1) and size frequency distribution (grouped into 5 mm shell length classes) of Dosinia

exoleta from Aveiro, Setubal and Faro during the fishing surveys performed by IPIMAR along the Portuguese coast in 2010

Helgol Mar Res (2013) 67:639–652 649

123

fishery management measures. The present study provided

the first data available on the growth parameters of

D. exoleta, but further studies should be conducted, namely

the estimation of the size at first sexual maturity, decisive

for establishing a minimum landing size for the catches of

this species by the bivalve dredging fleet that operates in

northern Portugal.

Acknowledgments The authors would like to acknowledge the

technical staff of the IPIMAR’s Delegation of Aveiro for collecting

and sampling the bivalves. Recognition is owed to Cte. Ventura So-

ares (Technical Director of the–IH) for kindly providing data on

seawater temperature. Thanks are also due to Joao Curdia for pho-

tographing the acetate peel replicas of the shells. Paulo Vasconcelos

is funded by a post-doctoral Grant (SFRH/BPD/26348/2006) awarded

by the Fundacao para a Ciencia e Tecnologia (FCT–Portugal). This

study was performed within the framework of the project ‘‘Desarrollo

Sostenible de las Pesquerıas Artesanales del Arco Atlantico–PRE-

SPO’’ (Programme INTERREG IV B, co-financed by EU, ERDF

funds). Finally, the authors also acknowledge two anonymous

reviewers, for valuable comments and suggestions that improved the

revised version of the manuscript.

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